Patterns and evolution of nucleotide landscapes in seed plants

Abstract

Nucleotide landscapes, which are the way base composition is distributed along a genome, strongly vary among species. The underlying causes of these variations have been much debated. Though mutational bias and selection were initially invoked, GC-biased gene conversion (gBGC), a recombination-associated process favoring the G and C over A and T bases, is increasingly recognized as a major factor. As opposed to vertebrates, evolution of GC content is less well known in plants. Most studies have focused on the GC-poor and homogeneous Arabidopsis thaliana genome and the much more GC-rich and heterogeneous rice (Oryza sativa) genome and have often been generalized as a dicot/monocot dichotomy. This vision is clearly phylogenetically biased and does not allow understanding the mechanisms involved in GC content evolution in plants. To tackle these issues, we used EST data from more than 200 species and provided the most comprehensive description of gene GC content across the seed plant phylogeny so far available. As opposed to the classically assumed dicot/monocot dichotomy, we found continuous variations in GC content from the probably ancestral GC-poor and homogeneous genomes to the more derived GC-rich and highly heterogeneous ones, with several independent enrichment episodes. Our results suggest that gBGC could play a significant role in the evolution of GC content in plant genomes.

Figure 1.

Taxonomic (NCBI) Trees with Unbiased Mean GC Content at Third Codon Position (GC3) per Species and GC3 Distributions for Seven Representative Species. The mean GC3 of each species is plotted on the phylogenetic tree of seed plants. The height of the blue bars is proportional to mean GC3. The GC3 distribution is also plotted for seven representative species (x axis, GC3 in %; y axis, proportion of unigenes). Species colors: violet red, gymnosperms; turquoise, basal angiosperms; brown, noncommelinid monocots; orange, non-Poaceae commelinids; gold, Poaceae; and cadet blue, eudicots. Clade colors: violet red, gymnosperms; turquoise, basal angiosperms; yellow, monocots; and cadet blue, eudicots. The tree was plotted with the phylogenetic display and manipulation online tool Interactive Tree Of Life version 2 (Letunic and Bork, 2011).

Figure 2.

Box Plots of Mean GC per Species by Taxonomic Group. (A) to (E) Box plots showing the among-species variations of GC content at different coding and UTR positions for six taxonomic groups. On each box plot, the dark midline is the median, the bottom and top of the box are the lower and upper quartiles, respectively, and the ends of the whiskers are the lowest and highest data still within 1.5 times the interquartile range of the lower and higher quartiles, respectively. Significant differences between groups according to Kruskal-Wallis tests are indicated with letters. Bas, basal angiosperms; Com, non-Poaceae commelinids; Eud, eudicots; Gym, gymnosperms; Mon, noncommelinid monocots; Poa, Poaceae. (A) Mean GC1 (unbiased estimate). (B) Mean GC2 (unbiased estimate). (C) Mean GC3 (unbiased estimate). (D) Mean GC5UTR (raw estimate). (E) Mean GC3UTR (raw estimate).

Figure 3.

Unbiased sd GC3 as a Function of Unbiased Mean GC3. The scatterplot shows the strong positive correlation between GC richness (mean GC3) and GC heterogeneity (GC3 sd). Violet red, gymnosperms; turquoise, basal angiosperms; brown, noncommelinid monocots; orange, non-Poaceae commelinids; gold, Poaceae; cadet blue: eudicots. At, Arabidopsis; Os, O. sativa.

Figure 4.

Means of the Two Beta Distributions as a Function of Unbiased Mean GC3. The scatterplot shows that the means of the two Beta distributions correlate positively with the mean GC3. Squares, mean of the first Beta distribution; circles, mean of the second Beta distribution. Violet red, gymnosperms; turquoise, basal angiosperms; brown, noncommelinid monocots; orange, non-Poaceae commelinids; gold, Poaceae; cadet blue, eudicots. At, Arabidopsis; Os, O. sativa.

Figure 5.

Spearman’s Rho between GC3 and Expression Level. The box plot shows that GC3 is positively correlated with expression level in most species, irrespective of their taxonomic group. Only species with significant correlation (Spearman’s test, P value ≤ 0.05) were plotted. On each box plot, the dark midline is the median, the bottom and top of the box are the lower and upper quartiles, respectively, and the ends of the whiskers are the lowest and highest data still within 1.5 times the interquartile range of the lower and higher quartiles, respectively. The number of species with significant correlation (S) and nonsignificant correlation (NS) is indicated below the graphs. Significant differences between groups according to Kruskal-Wallis tests are indicated with letters. Bas, basal angiosperms; Com, non-Poaceae commelinids; Eud, eudicots; Gym, gymnosperms; Mon, noncommelinid monocots; Poa, Poaceae.

Figure 6.

Spearman’s Rho between Local GC3 and GC1 and between Local GC3 and GC2: Box Plots and Plots as Functions of Unbiased Mean GC3. (A) and (B) Box plots of Spearman’s correlation coefficients between GC1 and GC3 (A) and GC2 and GC3 (B) within the genome for six taxonomic groups (C) and (D) Scatterplots of Spearman’s correlation coefficients between GC1 and GC3 (C) and GC2 and GC3 (D) as a function of mean GC3. Only species with significant correlation (Spearman’s test, P value ≤ 0.05) were plotted. On each box plot, the dark midline is the median, the bottom and top of the box are the lower and upper quartiles, respectively, and the ends of the whiskers are the lowest and highest data, respectively, still within 1.5 times the interquartile range of the lower and higher quartiles, respectively. The number of species with significant correlation (S) and nonsignificant correlation (NS) are indicated below the graphs. Significant differences between groups according to Kruskal-Wallis tests are indicated with letters. Violet red, gymnosperms (Gym); turquoise, basal angiosperms (Bas); brown, noncommelinid monocots (Mon); orange, non-Poaceae commelinids (Com); gold, Poaceae (Poa); cadet blue, eudicots (Eud).

Figure 7.

GC3 Gradients along Transcripts as a Function of Mean GC3. The scatterplot shows the strong correlation between GC richness (mean GC3) and the steepness of the GC gradient along transcripts. Violet red, gymnosperms; cadet blue, eudicots; gold, monocots (Poaceae). At, Arabidopsis; Os, O. sativa.

Figure 8.

Relationship between Local Recombination Rate and GC3 in Three Grass Species. The scatterplot shows the strong positive correlation between local recombination rate and GC3 in three grass species. Genes have been grouped into 20 bins according to their local recombination rate. Dots correspond to the mean GC3 of each bin and bars to the ses. Black dots, B. distachyon; gray dots, maize; white dots, rice.